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Potential Mechanisms of Enteric Cytoprotection by Probiotics: Lessons from Cultured Human Intestinal Cells

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Probiotic Bacteria and Enteric Infections

Abstract

Probiotic lactic acid strains are defined as live microorganisms which, when consumed in appropriate amounts in food, confer a health benefit on the host (FAO/WHO 2001, 2002). These strains include lactobacilli and bifidobacteria, which are commercialized as food or dietary supplements of living bacteria, and have attracted the interest of scientists as well as consumers (Gorbach 2000; Mercenier et al. 2003; Picard et al. 2005; Saxelin et al. 2005; Reid and Bruce 2006; Blandino et al. 2008; Koninkx and Malago 2008; Preidis and Versalovic 2009). One of the advantages of repeatedly consuming probiotic lactic acid bacteria in appropriate amounts could be that they maintain a higher, albeit generally transient, bacterial density in the upper part of the intestinal tract, a location that normally hosts very few resident microbiota bacteria, and in which enteric Gram-negative pathogens produce their harmful effects. The number and activity of live bacteria present in probiotic preparations sometimes declines if they are stored for inappropriate times and/or at inappropriate temperatures.

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References

  • Abreu MT, Fukata M, Arditi M (2005) TLR signaling in the gut in health and disease. J Immunol 174:4453–4460

    PubMed  CAS  Google Scholar 

  • Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511

    Article  PubMed  CAS  Google Scholar 

  • Augeron C, Voisin T, Maoret JJ, Berthon B, Laburthe M, Laboisse CL (1992) Neurotensin and neuromedin N stimulate mucin output from human goblet cells (Cl.16E) via neurotensin receptors. Am J Physiol 262:G470–G476

    PubMed  CAS  Google Scholar 

  • Ayabe T, Ashida T, Kohgo Y, Kono T (2004) The role of Paneth cells and their antimicrobial peptides in innate host defense. Trends Microbiol 12:394–398

    Article  PubMed  CAS  Google Scholar 

  • Bai AP, Ouyang Q, Zhang W, Wang CH, Li SF (2004) Probiotics inhibit TNF-alpha-induced interleukin-8 secretion of HT29 cells. World J Gastroenterol 10:455–457

    PubMed  CAS  Google Scholar 

  • Banerjee P, Merkel GJ, Bhunia AK (2009) Lactobacillus delbrueckii ssp. bulgaricus B-30892 can inhibit cytotoxic effects and adhesion of pathogenic Clostridium difficile to Caco-2 cells. Gut Pathog 1:8

    Article  PubMed  CAS  Google Scholar 

  • Baricault L, Denariaz G, Houri JJ, Bouley C, Sapin C, Trugnan G (1995) Use of HT-29, a cultured human colon cancer cell line, to study the effect of fermented milks on colon cancer cell growth and differentiation. Carcinogenesis 16:245–252

    Article  PubMed  CAS  Google Scholar 

  • Blandino G, Fazio D, Di Marco R (2008) Probiotics: overview of microbiological and immunological characteristics. Expert Rev Anti Infect Ther 6:497–508

    Article  PubMed  CAS  Google Scholar 

  • Boirivant M, Strober W (2007) The mechanism of action of probiotics. Curr Opin Gastroenterol 23:679–692

    Article  PubMed  Google Scholar 

  • Borthakur A et al (2008) The probiotic Lactobacillus acidophilus stimulates chloride/hydroxyl exchange activity in human intestinal epithelial cells. J Nutr 138:1355–1359

    PubMed  CAS  Google Scholar 

  • Caballero-Franco C, Keller K, De Simone C, Chadee K (2007) The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol 292:G315–G322

    Article  PubMed  CAS  Google Scholar 

  • Camp JG, Kanther M, Semova I, Rawls JF (2009) Patterns and scales in gastrointestinal microbial ecology. Gastroenterology 136:1989–2002

    Article  PubMed  Google Scholar 

  • Candela M et al (2008) Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol 125:286–292

    Article  PubMed  CAS  Google Scholar 

  • Cario E, Podolsky DK (2005) Intestinal epithelial TOLLerance versus inTOLLerance of commensals. Mol Immunol 42:887–893

    Article  PubMed  CAS  Google Scholar 

  • Chantret I et al (1994) Differential expression of sucrase-isomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation. J Cell Sci 107(Pt 1):213–225

    PubMed  CAS  Google Scholar 

  • Clark MA, Jepson MA (2003) Intestinal M cells and their role in bacterial infection. Int J Med Microbiol 293:17–39

    Article  PubMed  CAS  Google Scholar 

  • Coburn B, Grassl GA, Finlay BB (2007) Salmonella, the host and disease: a brief review. Immunol Cell Biol 85:112–118

    Article  PubMed  Google Scholar 

  • Coconnier MH, Liévin V, Lorrot M, Servin AL (2000) Antagonistic activity of Lactobacillus acidophilus LB against intracellular Salmonella enterica serovar Typhimurium infecting human enterocyte-like Caco-2/TC-7 cells. Appl Environ Microbiol 66:1152–1157

    Article  PubMed  CAS  Google Scholar 

  • Coconnier-Polter MH, Liévin-Le Moal V, Servin AL (2005) A Lactobacillus acidophilus strain of human gastrointestinal microbiota origin elicits killing of enterovirulent Salmonella enterica Serovar Typhimurium by triggering lethal bacterial membrane damage. Appl Environ Microbiol 71:6115–6120

    Article  PubMed  CAS  Google Scholar 

  • Collins SM, Bercik P (2009) The relationship between intestinal microbiota and the central nervous system in normal gastrointestinal function and disease. Gastroenterology 136:2003–2014

    Article  PubMed  Google Scholar 

  • Coron E et al (2009) Characterisation of early mucosal and neuronal lesions following Shigella flexneri infection in human colon. PLoS One 4:e4713

    Article  CAS  Google Scholar 

  • Cossart P, Toledo-Arana A (2008) Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect 10:1041–1050

    Article  PubMed  CAS  Google Scholar 

  • Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R (2009) Bacterial community variation in human body habitats across space and time. Science 326(5960):1694–1697

    Article  PubMed  CAS  Google Scholar 

  • Didierlaurent A, Sirard JC, Kraehenbuhl JP, Neutra MR (2002) How the gut senses its content. Cell Microbiol 4:61–72

    Article  PubMed  CAS  Google Scholar 

  • Ewaschuk JB, Backer JL, Churchill TA, Obermeier F, Krause DO, Madsen KL (2007) Surface expression of Toll-like receptor 9 is upregulated on intestinal epithelial cells in response to pathogenic bacterial DNA. Infect Immun 75:2572–2579

    Article  PubMed  CAS  Google Scholar 

  • Fagarasan S, Honjo T (2003) Intestinal IgA synthesis: regulation of front-line body defences. Nat Rev Immunol 3:63–72

    Article  PubMed  CAS  Google Scholar 

  • Fagarasan S, Honjo T (2004) Regulation of IgA synthesis at mucosal surfaces. Curr Opin Immunol 16:277–283

    Article  PubMed  CAS  Google Scholar 

  • Fantini J et al (1986) Spontaneous and induced dome formation by two clonal cell populations derived from a human adenocarcinoma cell line, HT29. J Cell Sci 83:235–249

    PubMed  CAS  Google Scholar 

  • FAO/WHO (2001) Joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Cordoba, Argentina, 1–4 Oct 2001. ftp://ftp.fao.org/docrep/fao/meeting/009/y6398e.pdf

    Google Scholar 

  • FAO/WHO (2002) Guidelines for the evaluation of probiotics in food. Food and agriculture organization of the unites nations and world health organization working group report. ftp://ftp.fao.org/es/esn/food/wgreport2.pdf

    Google Scholar 

  • Fogh J, Fogh JM, Orfeo T (1977) One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J Natl Cancer Inst 59:221–226

    PubMed  CAS  Google Scholar 

  • Franchi L, Warner N, Viani K, Nunez G (2009) Function of Nod-like receptors in microbial recognition and host defense. Immunol Rev 227:106–128

    Article  PubMed  CAS  Google Scholar 

  • Freitas M, Cayuela C, Antoine JM, Piller F, Sapin C, Trugnan G (2001) A heat labile soluble factor from Bacteroides thetaiotaomicron VPI-5482 specifically increases the galactosylation pattern of HT29-MTX cells. Cell Microbiol 3:289–300

    Article  PubMed  CAS  Google Scholar 

  • Freitas M, Tavan E, Cayuela C, Diop L, Sapin C, Trugnan G (2003) Host-pathogens cross-talk. Indigenous bacteria and probiotics also play the game. Biol Cell 95:503–506

    Article  PubMed  Google Scholar 

  • Furrie E, Macfarlane S, Thomson G, Macfarlane GT (2005) Toll-like receptors-2, -3 and -4 expression patterns on human colon and their regulation by mucosal-associated bacteria. Immunology 115:565–574

    Article  PubMed  CAS  Google Scholar 

  • Ganz T (2001) Antimicrobial proteins and peptides in host defense. Semin Respir Infect 16:4–10

    Article  PubMed  CAS  Google Scholar 

  • Garrett WS et al (2007) Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 131:33–45

    Article  PubMed  CAS  Google Scholar 

  • Gorbach SL (2000) Probiotics and gastrointestinal health. Am J Gastroenterol 95:S2–S4

    Article  PubMed  CAS  Google Scholar 

  • Granato D et al (1999) Cell surface-associated lipoteichoic acid acts as an adhesion factor for attachment of Lactobacillus johnsonii La1 to human enterocyte-like Caco-2 cells. Appl Environ Microbiol 65:1071–1077

    PubMed  CAS  Google Scholar 

  • Heuvelin E, Lebreton C, Grangette C, Pot B, Cerf-Bensussan N, Heyman M (2009) Mechanisms involved in alleviation of intestinal inflammation by Bifidobacterium breve soluble factors. PLoS One 4:e5184

    Article  CAS  Google Scholar 

  • Hooper LV, Xu J, Falk PG, Midtvedt T, Gordon JI (1999) A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc Natl Acad Sci U S A 96:9833–9838

    Article  PubMed  CAS  Google Scholar 

  • Hooper LV, Falk PG, Gordon JI (2000) Analyzing the molecular foundations of commensalism in the mouse intestine. Curr Opin Microbiol 3:79–85

    Article  PubMed  CAS  Google Scholar 

  • Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881–884

    Article  PubMed  CAS  Google Scholar 

  • Hooper LV, Midtvedt T, Gordon JI (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Ann Rev Nutr 22:283–307

    Article  CAS  Google Scholar 

  • Hooper LV, Stappenbeck TS, Hong CV, Gordon JI (2003) Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol 4:269–273

    Article  PubMed  CAS  Google Scholar 

  • Huang Y, Zheng Y (2009) The probiotic Lactobacillus acidophilus reduces cholesterol absorption through the down-regulation of Niemann-Pick C1-like 1 in Caco-2 cells. Br J Nutr 103(4):473–478

    Article  PubMed  CAS  Google Scholar 

  • Huet C, Sahuquillo-Merino C, Coudrier E, Louvard D (1987) Absorptive and mucus-secreting subclones isolated from a multipotent intestinal cell line (HT-29) provide new models for cell polarity and terminal differentiation. J Cell Biol 105:345–357

    Article  PubMed  CAS  Google Scholar 

  • Imaoka A et al (2008) Anti-inflammatory activity of probiotic Bifidobacterium: enhancement of IL-10 production in peripheral blood mononuclear cells from ulcerative colitis patients and inhibition of IL-8 secretion in HT-29 cells. World J Gastroenterol 14:2511–2516

    Article  PubMed  CAS  Google Scholar 

  • Johnson-Henry KC, Donato KA, Shen-Tu G, Gordanpour M, Sherman PM (2008) Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157:H7-induced changes in epithelial barrier function. Infect Immun 76:1340–1348

    Article  PubMed  CAS  Google Scholar 

  • Kaper JB, Nataro JP, Mobley HL (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2:123–140

    Article  PubMed  CAS  Google Scholar 

  • Kelly D et al (2004) Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol 5:104–112

    Article  PubMed  CAS  Google Scholar 

  • Kelly D, Conway S, Aminov R (2005) Commensal gut bacteria: mechanisms of immune modulation. Trends Immunol 26:326–333

    Article  PubMed  CAS  Google Scholar 

  • Klingberg TD, Pedersen MH, Cencic A, Budde BB (2005) Application of measurements of transepithelial electrical resistance of intestinal epithelial cell monolayers to evaluate probiotic activity. Appl Environ Microbiol 71:7528–7530

    Article  PubMed  CAS  Google Scholar 

  • Ko JS, Yang HR, Chang JY, Seo JK (2007) Lactobacillus plantarum inhibits epithelial barrier dysfunction and interleukin-8 secretion induced by tumor necrosis factor-alpha. World J Gastroenterol 13:1962–1965

    PubMed  CAS  Google Scholar 

  • Koninkx JF, Malago JJ (2008) The protective potency of probiotic bacteria and their microbial products against enteric infections—review. Folia Microbiol 53:189–194

    Article  CAS  Google Scholar 

  • Korhonen R, Kosonen O, Korpela R, Moilanen E (2004) The expression of COX2 protein induced by Lactobacillus rhamnosus GG, endotoxin and lipoteichoic acid in T84 epithelial cells. Lett Appl Microbiol 39:19–24

    Article  PubMed  CAS  Google Scholar 

  • Kraehenbuhl JP, Neutra MR (2000) Epithelial M cells: differentiation and function. Ann Rev Cell Dev Biol 16:301–332

    Article  CAS  Google Scholar 

  • Kreusel KM, Fromm M, Schulzke JD, Hegel U (1991) Cl-secretion in epithelial monolayers of mucus-forming human colon cells (HT-29/B6). Am J Physiol 261:C574–C582

    PubMed  CAS  Google Scholar 

  • Laboisse C, Jarry A, Branka JE, Merlin D, Bou-Hanna C, Vallette G (1995) Regulation of mucin exocytosis from intestinal goblet cells. Biochem Soc Trans 23:810–813

    PubMed  CAS  Google Scholar 

  • Lammers KM et al (2002) Effect of probiotic strains on interleukin 8 production by HT29/19A cells. Am J Gastroenterol 97:1182–1186

    Article  PubMed  CAS  Google Scholar 

  • Langefeld T, Mohamed W, Ghai R, Chakraborty T (2009) Toll-like receptors and NOD-like receptors: domain architecture and cellular signalling. Adv Exp Med Biol 653:48–57

    Article  PubMed  CAS  Google Scholar 

  • Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72:728–764 (Table of Contents)

    Article  PubMed  CAS  Google Scholar 

  • Lenoir C et al (2008) MD-2 controls bacterial lipopolysaccharide hyporesponsiveness in human intestinal epithelial cells. Life Sci 82:519–528

    Article  PubMed  CAS  Google Scholar 

  • Lesuffleur T et al (1991) Increased growth adaptability to 5-fluorouracil and methotrexate of HT- 29 sub-populations selected for their commitment to differentiation. Int J Cancer 49:731–737

    Article  PubMed  CAS  Google Scholar 

  • Ley RE et al (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651

    Article  PubMed  CAS  Google Scholar 

  • Liévin-Le Moal V, Amsellem R, Servin AL, Coconnier MH (2002) Lactobacillus acidophilus (strain LB) from the resident adult human gastrointestinal microflora exerts activity against brush border damage promoted by a diarrhoeagenic Escherichia coli in human enterocyte-like cells. Gut 50:803–811

    Article  Google Scholar 

  • Liévin-Le Moal V, Servin AL (2006) The front line of enteric host defence against unwelcome intrusion of harmful microorganisms: mucins, antimicrobioal peptides and microbiota. Clin Microbiol Rev 19(2):315–337

    Article  CAS  Google Scholar 

  • Liévin-Le Moal V, Sarrazin-Davila LE, Servin AL (2007) An experimental study and a randomized, double-blind, placebo-controlled clinical trial to evaluate the antisecretory activity of Lactobacillus acidophilus strain LB against nonrotavirus diarrhoea. Pediatrics 120:e795–e803

    Article  Google Scholar 

  • Lindfors K et al (2008) Live probiotic Bifidobacterium lactis bacteria inhibit the toxic effects induced by wheat gliadin in epithelial cell culture. Clin Exp Immunol 152:552–558

    Article  PubMed  CAS  Google Scholar 

  • Liu TS et al (2003) Protective role of HSP72 against Clostridium difficile toxin A-induced intestinal epithelial cell dysfunction. Am J Physiol Cell Physiol 284:C1073–C1082

    Google Scholar 

  • Lopez-Boado YS, Wilson CL, Hooper LV, Gordon JI, Hultgren SJ, Parks WC (2000) Bacterial exposure induces and activates matrilysin in mucosal epithelial cells. J Cell Biol 148:1305–1315

    Article  PubMed  CAS  Google Scholar 

  • Louvard D, Kedinger M, Hauri HP (1992) The differentiating intestinal epithelial cell: establishment and maintenance of functions through interactions between cellular structures. Ann Rev Cell Biol 8:157–195

    Article  PubMed  CAS  Google Scholar 

  • Ma D, Forsythe P, Bienenstock J (2004) Live Lactobacillus reuteri is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infect Immun 72:5308–5314

    Article  PubMed  CAS  Google Scholar 

  • Mack DR, Michail S, Wei S, McDougall L, Hollingsworth MA (1999) Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am J Physiol 276:G941–G950

    PubMed  CAS  Google Scholar 

  • Mack DR, Ahrne S, Hyde L, Wei S, Hollingsworth MA (2003) Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut 52:827–833

    Article  PubMed  CAS  Google Scholar 

  • Madara JL, Stafford J, Dharmsathaphorn K, Carlson S (1987) Structural analysis of a human intestinal epithelial cell line. Gastroenterology 92:1133–1145

    PubMed  CAS  Google Scholar 

  • Mattar AF, Teitelbaum DH, Drongowski RA, Yongyi F, Harmon CM, Coran AG (2002) Probiotics up-regulate MUC-2 mucin gene expression in a Caco-2 cell-culture model. Pediatr Surg Int 18:586–590

    Article  PubMed  CAS  Google Scholar 

  • Matter K, Balda MS (2003) Functional analysis of tight junctions. Methods 30:228–234

    Article  PubMed  CAS  Google Scholar 

  • McCracken VJ, Lorenz RG (2001) The gastrointestinal ecosystem: a precarious alliance among epithelium, immunity and microbiota. Cell Microbiol 3:1–11

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov R (2001) Toll-like receptors and innate immunity. Nat Rev Immunol 1:135–145

    Article  PubMed  CAS  Google Scholar 

  • Menard S, Candalh C, Bambou JC, Terpend K, Cerf-Bensussan N, Heyman M (2004) Lactic acid bacteria secrete metabolites retaining anti-inflammatory properties after intestinal transport. Gut 53:821–828

    Article  PubMed  CAS  Google Scholar 

  • Mercenier A, Pavan S, Pot B (2003) Probiotics as biotherapeutic agents: present knowledge and future prospects. Curr Pharm Des 9:175–191

    Article  PubMed  CAS  Google Scholar 

  • Michail S, Abernathy F (2002) Lactobacillus plantarum reduces the in vitro secretory response of intestinal epithelial cells to enteropathogenic Escherichia coli infection. J Pediatr Gastroenterol Nutr 35:350–355

    Article  PubMed  CAS  Google Scholar 

  • Michail S, Abernathy F (2003) Lactobacillus plantarum inhibits the intestinal epithelial migration of neutrophils induced by enteropathogenic Escherichia coli. J Pediatr Gastroenterol Nutr 36:385–391

    Article  PubMed  Google Scholar 

  • Mizoguchi A, Mizoguchi E (2008) Inflammatory bowel disease, past, present and future: lessons from animal models. J Gastroenterol 43:1–17

    Article  PubMed  Google Scholar 

  • Montalto M et al (2004) Lactobacillus acidophilus protects tight junctions from aspirin damage in HT-29 cells. Digestion 69:225–228

    Article  PubMed  CAS  Google Scholar 

  • Moorthy G, Murali MR, Devaraj SN (2009) Lactobacilli facilitate maintenance of intestinal membrane integrity during Shigella dysenteriae 1 infection in rats. Nutrition 25:350–358

    Article  PubMed  CAS  Google Scholar 

  • Moriez R, Abdo H, Chaumette T, Faure M, Lardeux B, Neunlist M (2009) Neuroplasticity and neuroprotection in enteric neurons: role of epithelial cells. Biochem Biophys Res Commun 382:577–582

    Article  PubMed  CAS  Google Scholar 

  • Nandakumar NS, Pugazhendhi S, Madhu Mohan K, Jayakanthan K, Ramakrishna BS (2009) Effect of Vibrio cholerae on chemokine gene expression in HT29 cells and its modulation by Lactobacillus GG. Scand J Immunol 69:181–187

    Article  PubMed  CAS  Google Scholar 

  • Neudeck BL, Loeb JM, Faith NG (2004) Lactobacillus casei alters hPEPT1-mediated glycylsarcosine uptake in Caco-2 cells. J Nutr 134:1120–1123

    PubMed  CAS  Google Scholar 

  • Neunlist M et al (2003a) Toxin B of Clostridium difficile activates human VIP submucosal neurons, in part via an IL-1beta-dependent pathway. Am J Physiol Gastrointest Liver Physiol 285:G1049–G1055

    Google Scholar 

  • Neunlist M et al (2003b) Human ENS regulates the intestinal epithelial barrier permeability and a tight junction-associated protein ZO-1 via VIPergic pathways. Am J Physiol Gastrointest Liver Physiol 285:G1028–G1036

    Google Scholar 

  • O’Hara AM et al (2006) Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology 118:202–215

    Article  PubMed  CAS  Google Scholar 

  • Paolillo R, Romano Carratelli C, Sorrentino S, Mazzola N, Rizzo A (2009) Immunomodulatory effects of Lactobacillus plantarum on human colon cancer cells. Int Immunopharmacol 9:1265–1271

    Article  PubMed  CAS  Google Scholar 

  • Parassol N, Freitas M, Thoreux K, Dalmasso G, Bourdet-Sicard R, Rampal P (2005) Lactobacillus casei DN-114 001 inhibits the increase in paracellular permeability of enteropathogenic Escherichia coli-infected T84 cells. Res Microbiol 156:256–262

    Article  PubMed  CAS  Google Scholar 

  • Pasparakis M (2009) Regulation of tissue homeostasis by NF-kappaB signalling: implications for inflammatory diseases. Nat Rev Immunol 9:778–788

    Article  PubMed  CAS  Google Scholar 

  • Patel JC, Galan JE (2005) Manipulation of the host actin cytoskeleton by Salmonella—all in the name of entry. Curr Opin Microbiol 8:10–15

    Article  PubMed  CAS  Google Scholar 

  • Pedron T, Sansonetti P (2008) Commensals, bacterial pathogens and intestinal inflammation: an intriguing menage a trois. Cell Host Microbe 3:344–347

    Article  PubMed  CAS  Google Scholar 

  • Picard C, Fioramonti J, Francois A, Robinson T, Neant F, Matuchansky C (2005) Review article: bifidobacteria as probiotic agents—physiological effects and clinical benefits. Aliment Pharmacol Ther 22:495–512

    Article  PubMed  CAS  Google Scholar 

  • Pinto M et al (1983) Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol Cell 47:323–330

    Google Scholar 

  • Preidis GA, Versalovic J (2009) Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology 136:2015–2031

    Article  PubMed  CAS  Google Scholar 

  • Putaala H et al (2008) Effect of four probiotic strains and Escherichia coli O157:H7 on tight junction integrity and cyclo-oxygenase expression. Res Microbiol 159:692–698

    Article  PubMed  CAS  Google Scholar 

  • Qin H, Zhang Z, Hang X, Jiang Y (2009) L. plantarum prevents enteroinvasive Escherichia coli-induced tight junction proteins changes in intestinal epithelial cells. BMC Microbiol 9:63

    Article  PubMed  CAS  Google Scholar 

  • Reid G, Bruce AW (2006) Probiotics to prevent urinary tract infections: the rationale and evidence. World J Urol 24:28–32

    Article  PubMed  Google Scholar 

  • Resta-Lenert S, Barrett KE (2003) Live probiotics protect intestinal epithelial cells from the effects of infection with enteroinvasive Escherichia coli (EIEC). Gut 52:988–997

    Article  PubMed  CAS  Google Scholar 

  • Resta-Lenert S, Barrett KE (2006) Probiotics and commensals reverse TNF-alpha- and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology 130:731–746

    Article  PubMed  CAS  Google Scholar 

  • Riedel CU, Foata F, Philippe D, Adolfsson O, Eikmanns BJ, Blum S (2006) Anti-inflammatory effects of bifidobacteria by inhibition of LPS-induced NF-kappaB activation. World J Gastroenterol 12:3729–3735

    PubMed  Google Scholar 

  • Ropeleski MJ, Tang J, Walsh-Reitz MM, Musch MW, Chang EB (2003) Interleukin-11-induced heat shock protein 25 confers intestinal epithelial-specific cytoprotection from oxidant stress. Gastroenterology 124:1358–1368

    Article  PubMed  CAS  Google Scholar 

  • Roselli M, Finamore A, Britti MS, Mengheri E (2006) Probiotic bacteria Bifidobacterium animalis MB5 and Lactobacillus rhamnosus GG protect intestinal Caco-2 cells from the inflammation-associated response induced by enterotoxigenic Escherichia coli K88. Br J Nutr 95:1177–1184

    Article  PubMed  CAS  Google Scholar 

  • Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313–323

    Article  PubMed  CAS  Google Scholar 

  • Rousseaux C et al (2007) Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med 13:35–37

    Article  PubMed  CAS  Google Scholar 

  • Rouyer-Fessard C, Augeron C, Grasset E, Maoret JJ, Laboisse CL, Laburthe M (1989) VIP receptors and control of short circuit current in the human intestinal clonal cell line Cl.19A. Experientia 45:1102–1105

    CAS  Google Scholar 

  • Sanders ME, Hamilton J, Reid G, Gibson G (2007) A nonviable preparation of Lactobacillus acidophilus is not a probiotic. Clin Infect Dis 44:886

    Article  PubMed  Google Scholar 

  • Sands BE (2007) Inflammatory bowel disease: past, present, and future. J Gastroenterol 42:16–25

    Article  PubMed  Google Scholar 

  • Sansonetti PJ (2006) The bacterial weaponry: lessons from Shigella. Ann N Y Acad Sci 1072:307–312

    Article  PubMed  CAS  Google Scholar 

  • Sansonetti PJ (2008) Host-bacteria homeostasis in the healthy and inflamed gut. Curr Opin Gastroenterol 24:435–439

    Article  PubMed  Google Scholar 

  • Saxelin M, Tynkkynen S, Mattila-Sandholm T, de Vos WM (2005) Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol 16:204–211

    Article  PubMed  CAS  Google Scholar 

  • Schiffrin EJ, Blum S (2002) Interactions between the microbiota and the intestinal mucosa. Eur J Clin Nutr 56(Suppl 3):S60–S64

    Article  PubMed  Google Scholar 

  • Schlee M, Harder J, Koten B, Stange EF, Wehkamp J, Fellermann K (2008) Probiotic lactobacilli and VSL#3 induce enterocyte beta-defensin 2. Clin Exp Immunol 151:528–535

    Article  PubMed  CAS  Google Scholar 

  • Selsted ME, Ouellette AJ (2005) Mammalian defensins in the antimicrobial immune response. Nat Immunol 6:551–557

    Article  PubMed  CAS  Google Scholar 

  • Servin AL (2004) Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28:405–440

    Article  PubMed  CAS  Google Scholar 

  • Seth A, Yan F, Polk DB, Rao RK (2008) Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 294:G1060–G1069

    Article  CAS  Google Scholar 

  • Sherman PM, Johnson-Henry KC, Yeung HP, Ngo PS, Goulet J, Tompkins TA (2005) Probiotics reduce enterohemorrhagic Escherichia coli O157:H7- and enteropathogenic E. coli O127:H6-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements. Infect Immun 73:5183–5188

    Article  PubMed  CAS  Google Scholar 

  • Sonnenburg JL, Chen CT, Gordon JI (2006) Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol 4:e413

    Article  CAS  Google Scholar 

  • Tao Y et al (2006) Soluble factors from Lactobacillus GG activate MAPKs and induce cytoprotective heat shock proteins in intestinal epithelial cells. Am J Physiol Cell Physiol 290:C1018–C1030

    Google Scholar 

  • Tien MT et al (2006) Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epithelial cells. J Immunol 176:1228–1237

    PubMed  CAS  Google Scholar 

  • Toki S et al (2009) Lactobacillus rhamnosus GG and Lactobacillus casei suppress Escherichia coli-induced chemokine expression in intestinal epithelial cells. Int Arch Allergy Immunol 148:45–58

    Article  PubMed  CAS  Google Scholar 

  • Torres AG, Zhou X, Kaper JB (2005) Adherence of diarrhoeagenic Escherichia coli strains to epithelial cells. Infect Immun 73:18–29

    Article  PubMed  CAS  Google Scholar 

  • Turner JR (2009) Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9:799–809

    Article  PubMed  CAS  Google Scholar 

  • Vanderpool C, Yan F, Polk DB (2008) Mechanisms of probiotic action: Implications for therapeutic applications in inflammatory bowel diseases. Inflamm Bowel Dis 14:1585–1596

    Article  PubMed  Google Scholar 

  • Van Landeghem L et al (2009) Regulation of intestinal epithelial cells transcriptome by enteric glial cells: impact on intestinal epithelial barrier functions. BMC Genomics 10:507

    Article  PubMed  CAS  Google Scholar 

  • Vidal K, Donnet-Hughes A, Granato D (2002) Lipoteichoic acids from Lactobacillus johnsonii strain La1 and Lactobacillus acidophilus strain La10 antagonize the responsiveness of human intestinal epithelial HT29 cells to lipopolysaccharide and gram-negative bacteria. Infect Immun 70:2057–2064

    Article  PubMed  CAS  Google Scholar 

  • Viswanathan VK, Hodges K, Hecht G (2009) Enteric infection meets intestinal function: how bacterial pathogens cause diarrhoea. Nat Rev Microbiol 7:110–119

    PubMed  CAS  Google Scholar 

  • Vizoso Pinto MG, Schuster T, Briviba K, Watzl B, Holzapfel WH, Franz CM (2007) Adhesive and chemokine stimulatory properties of potentially probiotic Lactobacillus strains. J Food Prot 70:125–134

    PubMed  Google Scholar 

  • Vizoso Pinto MG, Rodriguez Gomez M, Seifert S, Watzl B, Holzapfel WH, Franz CM (2009) Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro. Int J Food Microbiol 133:86–93

    Article  PubMed  CAS  Google Scholar 

  • Voltan S et al (2008) Lactobacillus crispatus M247-derived H2O2 acts as a signal transducing molecule activating peroxisome proliferator activated receptor-gamma in the intestinal mucosa. Gastroenterology 135:1216–1227

    Article  PubMed  CAS  Google Scholar 

  • Wallace TD, Bradley S, Buckley ND, Green-Johnson JM (2003) Interactions of lactic acid bacteria with human intestinal epithelial cells: effects on cytokine production. J Food Prot 66:466–472

    PubMed  CAS  Google Scholar 

  • Xavier RJ, Podolsky DK (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448:427–434

    Article  PubMed  CAS  Google Scholar 

  • Xu J et al (2003) A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299:2074–2076

    Article  PubMed  CAS  Google Scholar 

  • Xu J et al (2007) Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol 5:e156

    Article  CAS  Google Scholar 

  • Yan F, Polk DB (2002) Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem 277:50959–50965

    Article  PubMed  CAS  Google Scholar 

  • Yan F, Cao H, Cover TL, Whitehead R, Washington MK, Polk DB (2007) Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132:562–575

    Article  PubMed  CAS  Google Scholar 

  • Zocco MA, Ainora ME, Gasbarrini G, Gasbarrini A (2007) Bacteroides thetaiotaomicron in the gut: molecular aspects of their interaction. Dig Liver Dis 39:707–712

    Article  PubMed  CAS  Google Scholar 

  • Zweibaum A et al (1985) Enterocytic differentiation of a subpopulation of the human colon tumor cell line HT-29 selected for growth in sugar-free medium and its inhibition by glucose. J Cell Physiol 122:21–29

    Article  PubMed  CAS  Google Scholar 

  • Zweibaum A, Laburthe M, Grasset E, Louvard D (1991) Use of cultured cell lines in studies of intestinal cell differentiation and function. In: Schultz SJ, Field FM, Frizell RA (eds) Handbook of physiology, the gastrointestinal system, intestinal absorption and secretion. American Physiological Society, Bethesda, pp 223–255

    Google Scholar 

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Correspondence to Alain L. Servin .

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Moal, V.LL., Servin, A.L. (2011). Potential Mechanisms of Enteric Cytoprotection by Probiotics: Lessons from Cultured Human Intestinal Cells. In: Malago, J., Koninkx, J., Marinsek-Logar, R. (eds) Probiotic Bacteria and Enteric Infections. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0386-5_16

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